sign in sign up
<<
Home , Restoration ecology

Integrating Ecological Knowledge into Restoration Management Liam Heneghan,1,2 Susan P. Miller,3 Sara Baer,4 Mac A. Callaham, Jr.,5 James Montgomery,1 Mitchell Pavao-Zuckerman,6 Charles C. Rhoades,7 and Sarah Richardson1

Abstract components of the soil system can be useful in the restora- The variability in the type of degradation and tion of a site, especially when the restoration goal is the specificity of restoration goals can challenge restora- loosely defined in terms of the species and processes that tionists’ ability to generalize about approaches that lead management seeks to achieve. These single-factor manip- to restoration success. The discipline of soil , which ulations may in fact produce cascading effects on several emphasizes both soil organisms and ecosystem processes, ecosystem attributes and can result in unintended recov- has generated a body of knowledge that can be generally ery trajectories. When complex outcomes are desired, useful in improving the outcomes of restoration despite intentional and holistic integration of all aspects of the soil this variability. Here, we propose that the usefulness of knowledge is necessary. We provide a short roster of ex- this soil ecological knowledge (SEK) for restoration is amples to illustrate that SEK benefits management and best considered in the context of the severity of the origi- restoration of and suggest areas for future nal perturbation, the goals of the project, and the resil- research. ience of the ecosystem to . A straightforward manipulation of single physical, chemical, or biological Key words: ecosystem processes, feedbacks, soil ecology.

Introduction et al. 2006). Published restoration science in the primary Restoration ecologists have long recognized the integral literature commonly includes soil information associated role of soil, particularly in its physical and chemical with pre-restoration site assessment and the evaluation of aspects, in the successful of degraded sites specific soil amendments (Callaham et al. 2008). Recovery (Jordan et al. 1987). However, explicit incorporation of of nutrient capital or biogeochemical processes also moti- soil ecological knowledge (SEK), which acknowledges vates restoration activities, but examples where integrated interactions among the principal components of the soil SEK has been employed are uncommon. system as well as feedback between the aboveground and In this article, we discuss restoration practice and re- belowground ecosystem processes, into restoration re- search that is informed by SEK. The term ‘‘soil ecological mains in a relatively early stage of development (Aronson knowledge’’ is used to indicate perspectives from the disci- et al. 1993; Harris et al. 2006; Wardle & Peltzer 2007). pline of soil ecology that integrate soil physical, chemical, Despite earlier attempts to demonstrate the importance of and biological factors and processes in context of – a soil’s perspective for restoration efforts, a recent and soil feedback. In particular, it is knowledge from soil useful review of research on makes ecology that can be used explicitly to inform restoration only scattered references to soil processes and biota (Falk practice. A restoration approach that employs more sophisticated SEK differs from simpler approaches that consider soil factors in isolation or that separates above- 1 DePaul University, Environmental Science Program, Chicago, IL 60614, U.S.A. ground from belowground ecosystem processes. We dis- 2 Address correspondence to L. Heneghan, email [email protected] cuss a classification of restoration approaches arrayed 3 Millroad Ecological Services, 2200 Three Oaks Court, Fort Collins, CO 80526, U.S.A. along a gradient of increasing need for knowledge of soil 4 Department of Plant Biology, Southern Illinois University, Carbondale, ecology to attain the ecosystem structure and function of IL 62901, U.S.A. 5 USDA-Forest Service, Forestry Sciences Laboratory, Athens, GA 30602, a particular reference condition. Additionally, we identify U.S.A. promising new research areas, where restoration projects 6 Biosphaere 2, PO Box 210088, University of Arizona, Tucson, AZ 85721, U.S.A. may advance our understanding of soil ecology and where, 7 USDA Forest Service Rocky Mountain Research Station, Fort Collins, reciprocally, a deepened knowledge of the soil system CO 80526, U.S.A. may enhance restoration practice.

Ó 2008 Society for Ecological Restoration International The discipline of soil ecology has deep roots in soil sci- doi: 10.1111/j.1526-100X.2008.00477.x ence and organismal biology. Soil ecologists have merged

608 Restoration Ecology Vol. 16, No. 4, pp. 608–617 DECEMBER 2008 Integrating Soil Ecological Knowledge these traditional disciplines to understand ecosystem pro- cesses, which have provided tools for elucidating concepts central to ecology as a whole (Coleman et al. 2004; Lavelle & Spain 2001; Bardgett 2005). For example, rela- tionships between and ecosystem functioning have been tested using model soil ecosystems (Lavelle 1996; Bengtsson 1998; Lawton et al. 1998; Setala et al. 1998; Behan-Pelletier & Newton 1999; Heneghan et al. 1999; Zak et al. 2003; Fitter et al. 2005). Furthermore, perspectives in soil ecology that focus on the reciprocal feedback of above- and belowground biota and pro- cesses have become increasingly central to ecology (e.g., Casper & Jackson 1997; Klironomos 2002; Setala 2002; Wardle 2002; Bardgett & Wardle 2003; Van Der Putten 2003; Wardle et al. 2004). The holistic perspective that integrates organismic and ecosystem processes at the core of soil ecology has provided explanations for patterns in the distribution, , and composi- tion of species, a fundamental organizing tenet in ecol- ogy (Tilman 1982; Bever 1994; Bever et al. 1997; Baer et al. 2005). Soil biota is directly involved in key ecosystem pro- cesses (e.g., and nutrient cycling), and understanding such interactions has provided one of the unifying themes of soil ecological research over the past few decades (Swift et al. 1979; Wardle 2002). Because of the demonstrated key role in the regulation of ecosystem processes, application of insights from soil ecology has been useful in situations where desired outcomes go beyond simple enhancement of single factors such as pro- ductivity. For instance, soil ecology has made a substantial contribution to alternative agricultural practices, such as no-till cropping systems, by integrating conservation of physical, chemical, and biological properties of soil Figure 1. Framework for linking (a) SEK to existing theoretical (Coleman et al. 2002). In this case, soil ecologists have models of ecosystem restoration (b and c). (a) When sites are heavily demonstrated the importance of shifts from bacterial to degraded, improved soil function may be achieved by simple single- fungal channels in soil food webs for the development of factor manipulations of a given chemical (C), physical (P), or bio- , soil organic matter (SOM) sequestration, logical (B) attribute. For greater progress toward a target condition, an increase in the degree of complex SEK is required (and the and modulation of soil nutrient availability (Hendrix et al. consideration of interactions between P, C, and B components will 1986; Beare et al. 1995). Lessons gained from agroecology be critical). (b) Physical and biological thresholds which must be have inspired recent investigations of changes in microbial overcome if restoration is to be successful (modified from Whisenant structure following cessation of tillage and 1999). (c) The integral relationship between structural and functional restoration of native vegetation (Allison et al. 2005; attributes in ecosystem restoration (modified from Bradshaw 1987). McKinley et al. 2005). See text for examples and further illustration.

Contribution of Soil Ecology to Restoration— characteristics of a specified reference condition. Signifi- A Classification cantly degraded sites generally require active consider- We propose that the relationship between SEK and resto- ation of the soil, e.g., remediating oil spills (Kuyukina ration may be best considered in the context of the sever- et al. 2003). Site remediation in circumstances where re- ity of the original perturbation, the goals of the project, storing pre-disturbance above- and belowground structure and the resilience of the original ecosystem to disturbance and function is not a priority and may require a mani- (Fig. 1). Our conceptual model builds on previous models pulation of a single physical, chemical, or biological part of ecosystem restoration (Bradshaw 1987; Whisenant of the soil system to improve a system’s state relative to 1999; Hobbs & Harris 2001). We surmise that the utility of the perturbed state. For example, when a system has been SEK for achieving a restoration goal depends on the so severely perturbed that simply will not grow degree to which the restoration intent aims to achieve (e.g., on contaminated by heavy metals, oil spills,

DECEMBER 2008 Restoration Ecology 609 Integrating Soil Ecological Knowledge brine scars), the restoration goal may be limited to Integration of Soil Knowledge: Case Studies reclaiming a specific structure or process to enable revege- Hobbs and Harris (2001) and Hobbs and Norton (2004) tation. This may be achieved through ripping, tilling, or suggest that abiotic and biotic constraints may stall the contouring compacted substrates to improve aeration, restorative process until thresholds are breached through infiltration, and root growth purposes (Ashby 1997; human intervention (Fig. 1b; Whisenant 1999; see Fig. 1). Jacinthe & Lal 2007); removing toxic chemicals; or The notion is that more degraded environments will altering pH (e.g., mine land reclamation). In some cases, require repairing the physical template (e.g., abiotic com- this can involve as little effort as essentially ‘‘waiting’’ for ponents) prior to restoring species composition (e.g., extant microbial populations to act on the offending tox- biotic components) and subsequently, the ecological func- ins. Some soil factors are known to be important in medi- tions representative of the reference system. Manipula- ating the availability of toxins to the microbes (e.g., soil tions directed at relieving abiotic filters can be physical porosity, sorption/desorption of toxins to organic matter, (e.g., reducing soil compaction), chemical (e.g., liming to pH, redox potential), and these factors are often targets alleviate acidity), or biological (e.g., using plants to stabi- for remediation (e.g., Mitsch & Jorgensen 2003). Such lize and remediate toxic chemical conditions [Shimp et al. approaches are shown in the lower left-hand part of Fig- 1993; Qadir et al. 2002]). ure 1a: the desired outcome is a relatively general one We suggest that management aimed at fully restoring the (getting some regrowth of vegetation), and the restora- ecosystem structure and function of a reference condition tionist may manipulate soil factors without requiring must integrate the physical, chemical, and biological factors a great deal of knowledge about interactions within of that system. We recognize that the soil is a proverbial the soil. ‘‘black box’’ where impacts of a given treatment are often Restoration in the sense of returning an ecosystem to evaluated by specific net outcomes despite the enormous a specified reference condition, e.g., a historical state, both complexity of interactions that may mediate the response in terms of a specific community structure and ecosystem and therefore determine those outcomes. For instance, function, will require an increasingly sophisticated under- manipulating a physical factor to alleviate compaction and standing of the soil and all its physical, chemical, and bio- promote greater plant production will likely simultaneously logical properties to achieve the desired goal. If a system alter a suite of aspects of the soil system, such as soil carbon is severely degraded, where soil food webs and processes storage (Jacinthe & Lal 2007). The use of thinning, burning, have been highly altered, an integrated consideration of and thinning plus burning as treatment variables in Ponder- physical, chemical, and biological properties of soil and osa pine increased total inorganic nitrogen availability in interactions between plants and soil will be required to treatments compared with untreated con- restore all components of the perturbed ecosystem to a ref- trols (Kaye & Hart 1998) and resulted in higher understory erence condition. This requirement for integrated SEK to diversity (Gundale et al. 2006). That is, the manipulation of achieve a specific desired system outcome is illustrated in the aboveground vegetation has well-characterized impacts the upper right-hand side of Figure 1a. on the cycling and storage of carbon and nutrient in the Finally, when the disturbance of a site is not so great as soil, and these cascades may be incorporated intentionally to overwhelm the resilience of a system (i.e., does not shift into management. Deliberate manipulation of soil that inte- it beyond the self-organized processes and structures of grates holistic knowledge of the soil system will be more the system [Gunderson 2000]), the need for management likely to achieve the restoration of several system functions intervention may be minimal. However, when the distur- or several aspects of community structure. For the purposes bance is such that the system is degraded to a relatively of illustrating the relative role of SEK in these examples, stable , the need for SEK will be we consider both and reclamation as types considerable. of ecological restoration. These will be considered along- Our model is summarized with a simple illustration side practices such as the manipulation of successional pro- (Fig. 1) in which an increasingly conscious integration of cesses, which are used to restore community composition physical, chemical, and biological factors is required as the and function to a particular reference condition. The exam- goal of approaching a specific desired ecological state is ples below illustrate a range of potential manipulations of reached. Management options exist along a gradient from physical, chemical, and biological factors available to the single-factor manipulations of physical, chemical, or restoration. In many cases, single manipulations targeted at biological elements (shown in Fig. 1a as P, C, and B in a physical, chemical, or biological component of the soil are separate circles) to ones where a deliberate regard for employed; in most cases, these manipulations have conse- a cascade of interrelated effects of manipulations of soil quences for other soil components though these are not factors (maximum SEK) is required to bring about a par- always fully understood. ticular outcome (shown as P, C, and B linked by arrows and bound together in a circle). We suggest that there are intermediate circumstances where a restoration outcome Physical Manipulations will require some knowledge of the interaction of effects Soil physical structure influences vegetation growth (shown as P, C, and B linked by arrows). (Passioura 1991). When soil structure is degraded, the

610 Restoration Ecology DECEMBER 2008 Integrating Soil Ecological Knowledge impacts, often mediated by a variety of other related soil community development and diversity (De Deyn et al. physical characteristics (including those that relate water 2004; Kardol et al. 2005). Soil biota include microflora availability), can affect both plant growth and community (i.e., bacteria and fungi), a wide range of functionally dis- composition (Burke et al. 1998; Kozlowski 1999). Physical tinct nematodes and microarthropods, as well as a variety manipulations to improve soil structure in highly degraded of macroinvertebrates (i.e., earthworms, beetle larvae, sites include a variety of tillage practices (e.g., disking, rip- cicadas). Numerous studies have examined the effects of ping, subsoiling; Scullion & Mohammed 1991; Ashby disturbance on soil microflora and fauna (e.g., Wardle 1997), incorporation of polyacrylamide beads (Vacher et al. 1995; Brussaard et al. 1997), and soil biota are com- et al. 2003), and topdressing (e.g., with nitrogenous fertil- monly employed as indicators of restoration success izers or with manure) (Ducsay & Lozek 2004; Johnson (Andersen & Sparling 1997; Todd et al. 2006; Callaham et al. 2006) (Callaham et al. 2008). Management of the et al. 2008). However, soil fauna have rarely been physical soil substrate depth influences the overall quan- directly manipulated to improve restoration success. One tity of water and nutrients available to support plant example of such manipulation is that of introducing growth (Binkley et al. 1995; Andrews et al. 1998; Bowen earthworms to improve soil porosity and aggregate et al. 2005). However, these often-effective practices can structure but with varying success (Butt 1999). Numer- be expensive and time consuming, making them impracti- ous studies have, however, directly manipulated mycor- cal for many restoration projects. rhizae, either through additions of spores, inoculation of plants, or addition of soil inocula from undisturbed communities. The use of mycorrhizal fungi in restora- Manipulation of Soil Chemistry/Fertility tion has attracted considerable attention in recent years, and increasingly sophisticated knowledge of the Fertilizers and chemical amendments are commonly used biology and ecology of this group of soil organisms can to improve restoration success (Lu et al. 1997; Jim 2001; influence restoration. Marrs 2002; Xia 2004). For instance, application of The community and ecosystem consequences of mycor- a phosphorus P fertilizer, N fertilizer, and lime, along rhizal infection vary with mycorrhizal dependency of the with appropriate pasture seed mix was needed to effec- dominant and rare species in a community (Bever et al. tively reestablish pasture in a New Zealand opencast coal 2001, 2002). For example, if dominant species depend on mine reclamation (Longhurst et al. 1999). Restoration of mycorrhizae, then their presence may be necessary for former agricultural land, with residually high levels of restoring ecosystem function (Richter & Stutz 2002). Res- inorganic nitrogen from long-term fertilization, may re- toration of rare species that are mycorrhizae dependent quire manipulations to reduce that favor the may require inoculation for establishment and achieving desired plant species adapted to nitrogen-limited systems the desired community composition (van der Heijden (Wilson & Gerry 1995; Paschke et al. 2000; Suding et al. et al. 1998). Likewise, inoculation may be necessary to 2004). reclaim extremely degraded sites and maximize productiv- Manipulation of soil chemistry and nutrition as part of ity of a limited under such circumstances ecosystem restoration is common, but consideration of (Frost et al. 2001). Incorporating mycorrhizae in restora- the consequences of these practices on physical and bio- tion requires an understanding of cascading ecological logical soil properties is rare (Callaham et al. 2008). For consequences from the relationship between belowground instance, the stated goal of treatments where topsoil or organisms, aboveground individuals, community structure, ‘‘topsoil substitute’’ is added is to improve soil nutrient and ecosystem processes. content and facilitate recovery of plant and com- Restoring mycorrhizae to degraded soils is difficult munity diversity (e.g., Torbert et al. 1990; Clewell 1999). (Cardoso & Kuyper 2006), and there is growing interest in However, these amendments also introduce plant seed, using commercial mycorrhizae inoculums to improve res- mycorrhizal symbionts, and soil microbes and alter soil toration success, which prompts a number of research microenvironment and water relations by changing soil questions. Are commercial fungi as effective and as viable texture, depth, density, and porosity. As such, these ‘‘sec- as native fungi (Caravaca et al. 2003; Querejeta et al. ondary’’ mechanisms may have significant influences on 2006; Tarbell & Koske 2007)? What are the risks associ- plant performance, the outcome of restoration activities. ated with using non-native fungi in restoration? Under We suggest that identification of these soil ecological what circumstance will they benefit invasive plants more mechanisms and interactions will substantially contribute than native plants (Schwartz et al. 2006)? to understanding of the controls on restoration success. Applying mycorrhizae requires knowledge about site conditions. Mycorrhizal fungi, for instance, may not grow at sites contaminated with heavy metals or where nutri- Manipulation of Soil Organisms ents are very low (Vosa´tka et al. 1999). Additionally, they Soil biota, both directly and indirectly, influence soil nutri- may also be inhibited by high levels of nutrients such as ent dynamics (Verhoef & Brussaard 1990; Lussenhop nitrogen from vehicles and fertilizers (Egerton-Warburton 1992; Brussaard et al. 1997) and can also influence plant et al. 2007). Although plants exhibit less dependence on

DECEMBER 2008 Restoration Ecology 611 Integrating Soil Ecological Knowledge mycorrhizae with increasing nutrient (P) availability in available and mineralized nitrogen has been shown to soil, an unpredictable benefit from sustained populations reduce colonization and cover of non- in is increased infection and plant survivorship during restorations (Baer et al. 2003). An integrative res- drought (Gemma et al. 2002; Allen et al. 2003; Walker toration approach may also involve physical and biological et al. 2004; Querejeta et al. 2006). strategies. For example, carbohydrate supplements along The use of mycorrhizae illustrates an important part of with prescribed fire enhanced native Australian tussock the SEK model: in order to effectively incorporate mycor- grass restoration (Prober et al. 2005). Baer et al. (2003) rhizae into a restoration strategy, a moderate level of found reduced colonization and cover of non-native spe- knowledge about the interactions between the physical, cies in soil amended with carbon to reduce nitrogen avail- chemical, and biological factors that prevail at a site is ability in a . Thus, carbon addition needed to drive the system along a trajectory leading to represents a tool with the potential to alleviate an impor- a specific outcome. tant filter (i.e., soil nitrogen fertility) on community assembly. Invasion of a system by exotic species may alter physi- Integrated Manipulation cal, chemical, and/or biological characteristics of the soil. In most of the examples presented above, the manipula- Recognizing feedbacks between invading plant species tion of one component of the soil has implications for and soil may be crucial to combating invasion. For exam- other components. Manipulations based upon an under- ple, Vinton and Goergen (2006) documented positive standing of such cascading effects can therefore be per- feedback between litter quality and nitrogen mineraliza- formed intentionally to achieve a particular restoration tion in grassland restoration invaded by Smooth brome result. In our model (Fig. 1), we propose that as the com- (Bromus inermis), a species that demands more nitrogen plexity and specificity of desired outcomes increase, inten- than native prairie grasses. Kulmatiski and Beard (2006) tionally integrated strategies become essential. Although found that soil manipulations (incorporation of activated many of the earliest restoration projects aimed at estab- carbon) influenced competitive interactions between inva- lishing vegetation of any sort, outcomes which specify sive and native plants in the soil by apparent sequestration complex species assemblages are now more prevalent of allelopathic compounds. Although their manipulations (Bradshaw 2004). As the restoration process approaches did not result in complete removal of invasive plants from desired functional and compositional attributes, we con- the system, their work demonstrated that solutions for this tend that a more nuanced understanding of SEK will type of complex restoration challenge require consider- be required. ation of complex soil processes. This type of targeted manipulation is relatively sophisticated and represents the most exciting future direction of research for soil ecolo- Integrated Manipulation of Soil physical, Chemical, and gists and restoration ecologists alike. Biological Properties: An Example Applying SEK to Combat Invasion To illustrate what integrated strategies (applying SEK) may resemble, we discuss efforts to produce resilient res- Soil Quality as a Concept Guiding Ecosystem toration outcomes in the face of sustained invasion by Restoration exotic species. Our conceptual scheme provides an opportunity for link- SEK has been increasingly applied to prevent and/or ing a soil’s perspective on restoration with monitoring of reduce invasion by exotic species in restoration. A sys- restoration progress using soil quality indices. Larson and tem’s susceptibility to invasion has been shown to increase Pierce (1991) defined soil quality as the capacity of a spe- in response to altered disturbance regime (e.g., woody cific kind of soil to function, within natural or managed encroachment in unburned grasslands) and/or soil re- ecosystem boundaries, to sustain plant and animal produc- source availability (Burke & Grime 1996; Davis et al. tivity, maintain or enhance water and air quality, and sup- 2000). For example, restoration of native grasslands on port human health and habitation. In the past 10 years, abandoned agricultural land can be impeded by years of research on the soil quality concept has proceeded rapidly, agricultural fertilizer inputs which have created soil nutri- with particular emphasis on understanding the role of the ent levels that favor invasive over native plant species soil in maintaining environmental quality (Glanz (McClendon & Redente 1992; Morghan & Seastedt 1999; 1995; Pickett et al. 2001) and on the application of the soil Maron & Jeffries 2001; Blumenthal et al. 2003; Averett quality concept to restoration and management of nonag- et al. 2004). The first step in restoring desired native plant ricultural lands (Sims et al. 1997; Singer & Ewing 2000; species or communities in such areas may therefore Karlen et al. 2001). require ‘‘defertilization’’ to export or sequester excess Soil quality is specific to each kind of soil (USDA- nutrients in order to optimize success of native plants that NRCS 2001); however, measuring dynamic soil properties demand lower soil nutrients. For example, the addition of such as SOM, soil structure, and water-holding capacity carbon, which promotes microbial immobilization of can be used both to compare the efficacy of different soil

612 Restoration Ecology DECEMBER 2008 Integrating Soil Ecological Knowledge management practices among soils on similar landscape complexity with all former functions of a specified refer- positions with equivalent inherent properties or to track ence condition, very targeted or specific SEK is needed. temporal changes on the same soil (Singer & Ewing 2000; Success in such instances will require a holistic approach, Karlen et al. 2001). The results of this assessment can then as even single-factor manipulations can affect soil physi- serve to guide subsequent soil management decisions cal, chemical, and biological properties. Variability in (Karlen et al. 2001). A variety of user-friendly qualitative the type of degradation, the specific restoration goals, and semiquantitative educational materials have been the time frame in which results are anticipated, and the developed for conducting soil quality assessments, includ- means by which outcomes are assessed challenge our ing a visual soil assessment procedure (Shepherd 2000), ability to generalize about approaches that lead to resto- Soil Quality Information Sheets (Muckel & Mausbach ration success. 1996), soil health scorecards (Romig et al. 1996), and com- Our conceptual scheme underscores a simple rule of mercially available soil quality test kits. thumb: when complex ecological outcomes are desired, Despite some criticism of the notion of soil quality, it incorporating a more comprehensive SEK is critical to should be noted that the soil quality concept was con- achieve restoration goals. The need for an adequate incor- ceived merely as an outreach and assessment tool for eval- poration of SEK into restoration practice may become even uating the sustainability of soil management practices and more pressing in future years in the face of global change for guiding decisions. It should be a suitable way (globalization of commerce, increased intercontinental flow of mediating between research on SEK and managers who of biota and materials, , etc.). The prospect may ultimately apply and evaluate the use of this informa- of climate change will force difficult decisions on where and tion in restoration projects. Considering the application of what may be restored in ecosystem restoration projects in the soil quality concept to restoration, Karlen et al. (2003) the future (Harris et al. 2006), and soil ecological considera- noted that soil quality assessment will be useful in quanti- tions may ultimately provide guidance for these decisions. fying both the resistance (defined as the capacity of a sys- This is evident, given the predicted changes to fundamental tem to continue functioning through a disturbance, Pimm characteristics of and processes in soils under different cli- 1984) of a soil to degradation and the resilience of a soil to mate change scenarios (Bellamy et al. 2005; Saxon et al. recover following degradation. Given its fundamental 2005). The implications of this for restoration are only now grounding in basic principles of pedology and soil ecology, being investigated (Fox 2007). the soil quality concept is inherently embedded in SEK Finally, as strong as is the potential for SEK to improve and, therefore, it can serve as a useful tool to guide ecosys- the practice of ecological restoration, the reciprocal influ- tem restoration. ences are also promising. Restoration aims to use ecologi- cal theory to improve practice and apply information from practice to improve theory (Palmer et al. 2006). Thus, con- Conclusions sidering soils in restoration will test our mechanistic understanding of the ecological structure and function of Restoration aims to overcome constraints on ecosystem soil in altered environments. Most importantly, this will recovery through natural processes to produce resilient expose deficiencies in our basic knowledge of soil ecology; ecosystems that are resistant to invasion, capture and as such, restoration practice provides an ‘‘acid test’’ for soil use resources efficiently, contain biological complexity ecology (Bradshaw 1987). needed to function effectively, and provide human-val- ued services (Ewel 1987; Hobbs 2006). Although the goal of each restoration is defined by stakeholders, selection of targets and assessment of success should be guided by Implications for Practice general theory from relevant disciplines and lessons from d Knowledge of soil should routinely be incorporated practice (Hobbs & Harris 2001). With this understand- into planning and evaluating restoration projects. ing, we contend that any attempt to facilitate ecosystem The level of sophistication required for incorporating recovery from degradation will be improved by applying SEK depends upon the extent of soil degradation, SEK. Soil ecological perspectives that have emerged in the goals of the project, and the resilience of the eco- recent decades are integrative and ecosystem oriented system, and therefore, all these factors need to be because they simultaneously consider the influence of considered in the execution of restoration work. soil physical, chemical, and biological structure on d When the goals of a restoration project are relatively energy flow and material cycling. SEK can be founda- general ones—e.g., revegetation of a degraded site, tional to restoration across multiple ecological scales without a specific target plant community planned— (from population to whole ecosystem restoration). We modest SEK will be needed. propose that the relevance of SEK to restoring degraded d However, restoring a highly degraded site to a very systems is determined by the level of soil degradation particular target condition will require extensive and the specificity of project goals. When a restoration SEK. project aims to restore highly degraded sites to a level of

DECEMBER 2008 Restoration Ecology 613 Integrating Soil Ecological Knowledge

Bengtsson, J. 1998. Which species? What kind of diversity? Which ecosys- d The field of soil ecology which has traditionally com- tem function? Some problems in studies of relations between bio- bined a strong organismal influence with a focus on diversity and ecosystem function. Applied Soil Ecology 10:191–199. ecosystem processes should provide a source of Bever, J. D. 1994. Feedback between plants and their soil communities in knowledge for restoration practitioners, while being an old field community. Ecology 75:1965–1977. itself influenced by knowledge emerging from resto- Bever, J. D. 2002. Negative feedback within a : host-specific ration practice. growth of mycorrhizal fungi reduces plant benefit. Proceedings of the Royal Society of London Series B-Biological Sciences 269:2595–2601. Bever, J. D., P. A. Schultz, A. Pringle, and J. B. Morton. 2001. Arbuscular mycorrhizal fungi: more diverse than meets the eye, and the ecologi- cal tale of why. BioScience 51:923–931. Acknowledgments Bever, J. D., K. M. Westover, and J. Antonovics. 1997. Incorporating the We thank two anonymous reviewers for useful comments soil community into plant : the utility of the feedback approach. Journal of Ecology 85:561–573. on the article. L. Heneghan gratefully acknowledges the Binkley, D., F. Suarez, C. Rhoades, R. Stottlemyer, and D. W. Valentine. support of National Park Service, Natural Resource Pro- 1995. Parent material depth controls ecosystem composition and gram Center during the preparation of this article. function on a riverside terrace in northwestern Alaska. Ecoscience 2:377–381. Blumenthal, D. M., N. R. Jordan, and M. P. Russelle. 2003. Soil carbon addition controls weeds and facilitates prairie restoration. Ecologi- LITERATURE CITED cal Applications 13:605–615. Allen, M. F., W. Swenson, J. I. Querejeta, L. M. Egerton-Warburton, and Bowen, C. K., G. E. Schuman, R. A. Olson, and L. J. Ingram. 2005. Influence K. K. Treseder. 2003. Ecology of mycorrhizae: a conceptual frame- of topsoil depth on plant and soil attributes of 24-year old reclaimed work for complex interactions among plants and fungi. Annual mined lands. Arid Land Research and Management 19:267–284. Review of Phytopathology 41:271–303. Bradshaw, A. 2004. The role of nutrients and the importance of function Allison, V. J., R. M. Miller, J. D. Jastrow, R. Matamala, and D. R. Zak. in the assembly of ecosystems. Pages 325–340 in V. M. Templeton, 2005. Changes in soil microbial community structure in a tallgrass R. Hobbs, T. H. Nuttle, and S. Halle, editors. and prairie chronosequence. Soil Science Society of America Journal restoration ecology: bridging the gap between theory and practice. 695:1412–1421. , Washington, D.C. Andersen, A. N., and G. P. Sparling. 1997. Ants as indicators of restoration Bradshaw, A. D. 1987. Restoration: an acid test for ecology. Pages 23–30 success: relationship with soil microbial biomass in the Australian in W. R. Jordan, M. E. Giplin, and J. D. Aber, editors. Restoration seasonal tropics. Restoration Ecology 5:109–114. ecology: a synthetic approach to ecological research. Cambridge Andrews, J. A., J. E. Johnson, J. L. Torbert, J. A. Burger, and D. L. Kelting. University Press, Cambridge, United Kingdom. 1998. Minesoil and site properties associated with early height growth Brussaard, L., V. M. Behan-Pelletier, D. E. Bignell, V. K. Brown, W. of eastern white pine. Journal of Environmental Quality 27:192–199. Didden, P. Folgarait, et al. 1997. Biodiversity and ecosystem func- Aronson, J., C. Floret, E. Le Floc’h, C. Ovalle, and R. Pontanier. 1993. tioning in soil. Ambio 26:563–570. Restoration and rehabilitation of degraded ecosystems in arid and Burke, I. C., W. K. Lauenroth, M. A. Vinton, P. B. Hook, R. H. Kelly, H. semi-arid lands. I. View from the South. Restoration Ecology, 1: E. Epstein, M. R. Aguiar, M. D. Robles, M. O. Aguilera, K. L. 8–17. Murphy, and R. A. Gill. 1998. Plant-soil interactions in temperate Ashby, W. C. 1997. Soil ripping and herbicides enhance tree and shrub grasslands. Biogeochemistry 42:121–143. restoration on stripmines. Restoration Ecology 5:169–177. Burke, M. J. W., and J. P. Grime. 1996. An experimental study of plant Averett, J. M., R. A. Klips, L. E. Nave, S. D. Frey, and P. S. Curtis. 2004. community invasibility. Ecology 77:776–790. Effects of soil carbon amendment on nitrogen availability and plant Butt, K. R. 1999. Inoculation of earthworms into reclaimed soils: the UK growth in an experimental restoration. Restoration experience. & Development 10:565–575. Ecology 12:568–574. Caravaca, F., J. M. Barea, J. Palenzuela, D. Figueroa, M. M. Alguacil, Baer, S. G., J. M. Blair, S. L. Collins, and A. K. Knapp. 2003. Soil resour- and A. Rolda´n. 2003. Establishment of shrub species in a degraded ces regulate and diversity in newly established tallgrass semiarid site after inoculation with native or allochthonous arbuscu- prairie. Ecology 84:724–735. lar mycorrhizal fungi. Applied Soil Ecology 22:103–111. Baer, S. G., S. L. Collins, J. M. Blair, A. K. Knapp, and A. K. Fiedler. Callaham, M., C. R. Rhoades, and L. Heneghan. 2008. A striking profile: 2005. Soil heterogeneity effects on tallgrass prairie community het- soils knowledge in restoration management and science. Restora- erogeneity: an application of ecological theory to restoration ecol- tion Ecology 16:604–607. ogy. Restoration Ecology 13:413–424. Cardoso, I. M., and T. W. Kuyper. 2006. Mycorrhizas and tropical soil fer- Bardgett, R. D. 2005. The biology of soil: a community and ecosystem tility. Ecosystems & Environment 116:72–84. approach. Oxford University Press, New York. Casper, B. B., and R. B. Jackson. 1997. Plant underground. Bardgett, R. D., and D. A. Wardle. 2003. -mediated linkages Annual Review of Ecology and Systematics 28:545–570. between aboveground and belowground communities. Ecology 84: Clewell, A. F. 1999. Restoration of riverine forest at Hall Branch on phos- 2258–2268. phate-mined land, Florida. Restoration Ecology 7:1–14. Beare,M.H.,D.C.Coleman,D.A.Crossley,P.F.Hendrix,andE.P. Coleman, D. C., D. A. Crossley, and P. F. Hendrix. 2004. Fundamentals Odum. 1995. A hierarchical approach to evaluating the significance of of soil ecology. Elsevier Academic Press, Oxford, United Kingdom. soil biodiversity to biogeochemical cycling. Plant and Soil 170:5–22. Coleman, D. C., S. L. Fu, P. Hendrix, and D. Crossley. 2002. Soil food- Behan-Pelletier, V., and G. Newton. 1999. Linking soil biodiversity and webs in agroecosystems: impacts of herbivory and tillage manage- ecosystem function: the taxonomic dilemma. BioScience 49:149–152. ment. European Journal of Soil Biology 38:21–28. Bellamy, P. H., P. J. Loveland, R. I. Bradley, R. M. Lark, and G. J. D. Davis, M. A., J. P. Grime, and K. Thompson. 2000. Fluctuating resources Kirk. 2005. Carbon losses from all soils across England and Wales in plant communities: A general theory of invasibility. Journal of 1978-2003. Nature 437:245–248. Ecology 88:528–534.

614 Restoration Ecology DECEMBER 2008 Integrating Soil Ecological Knowledge

De Deyn, G. B., C. E. Raaijmakers, and W. H. Van der Putten. 2004. Jordan, W., M. E. Giplin, and J. D. Aber, editors. 1987. Restoration ecol- Plant community development is affected by nutrients and soil ogy: a synthetic approach to ecological research. Cambridge Univer- biota. Journal of Ecology 92:824–834. sity Press, Cambridge, United Kingdom. Ducsay, L., and O. Lozek. 2004. Effect of topdressing with nitrogen on Kardol, P., T. M. Bezemer, A. van der Wal, and W. H. van der Putten. the yield and quality of winter wheat grain. Plant Soil and Environ- 2005. Successional trajectories of soil nematode and plant communi- ment 50:309–314. ties in a chronosequence of ex-arable lands. Biological Conservation Egerton-Warburton, L. M., N. C. Johnson, and E. B. Allen. 2007. 12:317–327. Mycorrhizal community dynamics following nitrogen fertilization: Karlen, D. L., S. S. Andrews, and J. W. Doran. 2001. Soil quality: current a cross-site test in five grasslands. Ecological Monographs 77: concepts and applications. Advances in Agronomy 74:1–40. 527–544. Karlen, D. L., S. S. Andrews, B. J. Weinhold, and J. W. Doran. 2003. Soil Ewel, J. J. 1987. Restoration is the ultimate test of ecological theory. quality: humankind’s foundation for survival. Journal of Soil and Pages 31–34 in W. R. Jordan, M. E. Giplin, and J. D. Aber, editors. Water Conservation 58:171–179. Restoration ecology: a synthetic approach to ecological research. Kaye, J. P., and S. C. Hart. 1998. Ecological restoration alters nitrogen Cambridge University Press, Cambridge, United Kingdom. transformations in a ponderosa pine bunchgrass ecosystem. Ecologi- Falk, D., M. Palmer, and J. B. Zedler, editors. 2006. Foundations of resto- cal Applications 8:1052–1060. ration ecology. Island Press, Washington, D.C. Klironomos, J. N. 2002. Feedback with soil biota contributes to plant rar- Fitter, A. H., C. A. Gilligan, K. Hollingworth, A. Kleczkowski, R. M. ity and invasiveness in communities. Nature 417:67–70. Twyman, J. W. Pitchford, and N. S. B. Programme. 2005. Biodiver- Kozlowski, T. T. 1999. Soil compaction and growth of woody plants. Scan- sity and ecosystem function in soil. 19: dinavian Journal of Forest Research 14:596–619. 369–377. Kulmatiski, A., and K. H. Beard. 2006. Activated carbon as a restoration Fox, D. 2007. Ecology—back to the no-analog future? Science 316:823. tool: potential for control of invasive plants in abandoned agricul- Frost, S. M., P. D. Stahl, and S. E. Williams. 2001. Long-term reestablish- tural fields. Restoration Ecology 14:251–257. ment of arbuscular mycorrhizal fungi in a drastically disturbed semi- Kuyukina, M. S., I. B. Ivshina, M. I. Ritchkova, J. C. Philp, C. J. Cunning- arid surface mine soil. Arid Land Research and Management 15: ham, and N. Christofi. 2003. Bioremediation of crude oil-contaminated 3–12. soil using slurry-phase biological treatment and land farming techni- Gemma, J. N., R. E. Koske, and M. Habte. 2002. Mycorrhizal dependency ques. Soil & Sediment Contamination 12:85–99. of some endemic and endangered Hawaiian plant species. American Larson, W. E., and F. J. Pierce. 1991. Conservation and enhancement of Journal of Botany 89:337–345. soil quality. Pages 175–203 in J. Dumanski, E. Pushparajah, M. Glanz, J. T. 1995. Saving our soil: solutions for sustaining ’s vital Latham, and R. Myers, editors. Evaluation for sustainable land resource. Johnson Books, Boulder, Colorado. management in the developing world. Vol. 2. Technical Papers. Gundale, M. J., K. L. Metlen, C. E. Fiedler, and T. H. DeLuca. 2006. Proceedings International Workshop. Chiang Rai, Thailand, 15–21 Nitrogen spatial heterogeneity influences diversity following resto- September 1991. International Board for Soil Research and Man- ration in a Ponderosa Pine Forest, Montana. Ecological Applica- agement, Bangkok, Thailand. tions 16:479–489. Lavelle, P. 1996. Diversity of soil fauna and ecosystem function. Biology Gunderson, L. H. 2000. —in theory and application. International 33:3–16. Annual Review of Ecology and Systematics 31:425. Lavelle, P., and A. Spain. 2001. Soil ecology. Kluwer Academic Publish- Harris, J. A., R. J. Hobbs, E. Higgs, and J. Aronson. 2006. Ecological res- ers, Dordrecht, The Netherlands. toration and global climate change. Restoration Ecology 14: Lawton, J. H., S. Naeem, L. J. Thompson, A. Hector, and M. J. Crawley. 170–176. 1998. Biodiversity and ecosystem function: getting the Ecotron Hendrix, P. F., R. W. Parmelee, D. A. Crossley Jr, and D. C. Coleman. experiment in its correct context. Functional Ecology 12:848–852. 1986. food webs in conventional and no-tillage agroecosys- Longhurst, R. D., M. B. O’Connor, and M. R. J. Toxopeus. 1999. Pasture tems. BioScience 36:374–380. establishment and fertiliser requirements on rehabilitated land after Heneghan, L., D. C. Coleman, X. Zou, D. A. Crossley, and B. L. Haines. opencast coal mining in New Zealand. New Zealand Journal of 1999. Soil microarthropod contributions to decomposition dynamics: Agricultural research 42:27–36. tropical-temperate comparisons of a single substrate. Ecology 80: Lu, J., M. J. Wilson, and J. Y. Yu. 1997. Effects of trench planting and soil 1873–1882. chiselling on soil properties and citrus production in hilly ultisols of Hobbs, R. J. 2006. Forward. Pages ix–x in D. A. Falk, M. A. Palmer, and China. Soil & Tillage Research 43:309–318. J.B. Zedler, editors. Foundations of restoration ecology. Island Lussenhop, J. 1992. Mechanisms of microarthropod microbial interactions Press, Washington, D.C. in soil. Advances in Ecological Research 23:1–33. Hobbs, R. J., and D. A. Norton. 2004. Ecological filters, thresholds Maron, J. L., and R. L. Jeffries. 2001. Restoring enriched grasslands: ef- and gradients in resistance to ecosystem reassembly. Pages 72–95 in fects of mowing on , productivity, and nitrogen V. Temperton, R. J. Hobbs, R. J. Halle, and M. Fattorini, eds. Assem- retention. Ecological Applications 11:1088–1100. bly rules and ecosystem restoration. Island Press, Washington, D.C. Marrs, R. H. 2002. Manipulating the chemical environment of the soil. Hobbs, R. J., and J. A. Harris. 2001. Restoration ecology: repairing the Pages 155–183 in M. R. Perrow and A. J. Davy, editors. Handbook Earth’s ecosystems in the new millennium. Restoration Ecology 9: of ecological restoration, vol. 1. Principles of restoration. Cambridge 239–246. University Press, Cambridge, United Kingdom. Jacinthe, P. A., and R. Lal. 2007. Carbon storage and minesoil properties McClendon, T., and E. F. Redente. 1992. Effects of nitrogen limitation on in relation to topsoil applications techniques. Soil Science Society of species replacement dynamics during early succession on a semiarid America Journal 71:1788–1795. sagebrush site. Oecologia 91:312–317. Jim, C. Y. 2001. Ecological and landscape rehabilitation of a site McKinley, V. L., A. D. Peacock, and D. C. White. 2005. Microbial in Hong Kong. Restoration Ecology 9:85–94. community PLFA and PHB responses to ecosystem restora- Johnson, N. C., J. D. Hoeksema, J. D. Bever, V. B. Chaudhary, C. tion in tallgrass prairie soils. Soil Biology & Biochemistry 37: Gehring, J. Klironomos, et al. 2006. From Lilliput to Brobdingnag: 1946–1958. extending models of mycorrhizal function across scales. BioScience Mitsch, W. J., and S. E. Jorgensen. 2003. : a field 56:889–900. whose time has come. Ecological Engineering 20:363–377.

DECEMBER 2008 Restoration Ecology 615 Integrating Soil Ecological Knowledge

Morghan, K. J. R., and T. R. Seastedt. 1999. Effects of soil nitrogen reduction Critical Reviews in Environmental Science and Technology 23: on nonnative plants in restored grasslands. Restoration Ecology 7:51–55. 41–77. Muckel, G. B., and M. J. Mausbach. 1996. Soil quality information sheets. Sims, J. T., S. D. Cunningham, and M. E. Sumner. 1997. Assessing soil Pages 393–400 in J. W. Doran, D. C. Coleman, D. F. Bezdicek, and quality for environmental purposes: roles and challenges for soil sci- B. A. Stewart, editors. Defining soil quality for a sustainable en- entists. Journal of Environmental Quality 26:20–25. vironment. SSSA Special Publication No. 35. Soil Science Society of Singer, M. J., and S. Ewing. 2000. Soil quality. Pages G-271–G-298 in America, Inc., and American society of Agronomy, Inc., Madison, M. E. Sumner, editor. Handbook of soil science. CRC Press, Boca Wisconsin. Raton, Florida. Palmer, M. A., D. A. Falk, and J. B. Zedler. 2006. Ecological theory and Suding, K. N., K. D. LeJeune, and T. R. Seastedt. 2004. Competitive im- restoration ecology. Pages 1–10 in D. A. Falk, M. A. Palmer, and J. pacts and responses of an invasive weed: dependencies on nitrogen B. Zedler, editors. Foundations of Restoration Ecology. Island and phosphorus availability. Oecologia 141:526–535. Press, Washington, D.C. Swift, M. J., O. W. Heal, and J. M. Anderson. 1979. Decomposition in ter- Paschke, M. W., T. McLendon, and E. F. Redente. 2000. Nitrogen availability restrial ecosystems. Blackwell, London, United Kingdom. and old-field succession in a shortgrass steppe. Ecosystems 3:144–158. Tarbell, T. J., and R. E. Koske. 2007. Evaluation of commercial arbuscu- Passioura, J. B. 1991. Soil structure and plant-growth. Australian Journal lar mycorrhizal inocula in a sand/peat medium. Mycorrhiza 18: of Soil Research 29:717–728. 51–56. Pickett, S. T. A., M. L. Cadenasso, J. M. Grove, C. H. Nilon, R. V. Tilman, D. 1982. Resource competition and community structure. Mono- Pouyat, W. C. Zipperer, and R. Costanza. 2001. Urban ecological graphs in Population Biology, Princeton University Press, Princeton, systems: linking terrestrial, ecological, physical, and socioeconomic New Jersey. components of metropolitan areas. Annual Review of Ecology and Todd, T. C., T. O. Powers, and P. G. Mullin. 2006. Sentinel nematodes Systematics 21:127–157. of land-use change and restoration in tallgrass prairie. Journal of Pimm, S. L. 1984. The complexity and stability of ecosystems. Nature 307: Nematology 38:20–27. 321–326. Torbert, J. L., J. A. Burger, and W. L. Daniels. 1990. Pine growth varia- Prober, S. M., K. R. Thiele, I. D. Lunt, and T. B. Koen. 2005. Restoring tion associated with overburden rock type on a reclaimed surface ecological function in temperate grassy woodlands: manipulating mine in Virginia. Journal of Environmental Quality 19:88–92. soil nutrients, exotic annuals and native perennial grasses through USDA-NRCS (United States Department of Agriculture-Natural Re- carbon supplements and spring burns. Journal of sources Conservation Service). 2001. Guidelines for soil quality 42:1073–1085. assessment in conservation planning. USDA-NRCS-Soil Quality Qadir, M., R. H. Qureshi, and N. Ahmad. 2002. Amelioration of calcare- Institute, Ames, Iowa. ous saline sodic soils through phytoremediation and chemical strate- Vacher, C. A., R. J. Loch, and S. R. Raine. 2003. Effect of polyacrylamide gies. Soil Use and Management 18:381–385. additions on infiltration and of disturbed lands. Australian Querejeta, J. I., M. F. Allen, F. Caravaca, and A. Roldan. 2006. Differen- Journal of Soil Research 41:1509–1520. tial modulation of host plant delta C-13 and delta O-18 by native van der Heijden, M. G. A., J. N. Klironomos, M. Ursic, P. Moutoglis, and nonnative arbuscular mycorrhizal fungi in a semiarid environ- R. Streitwolf-Engel, T. Boller, A. Wiemken, and I. R. Sanders. ment. New Phytologist 169:379–387. 1998. Mycorrhizal fungal diversity determines plant biodiversity, Richter, B. S., and J. C. Stutz. 2002. Mycorrhizal inoculation of big saca- ecosystem variability and productivity. Nature 396:69–72. ton: implications for grassland restoration of abandoned agricultural Van Der Putten, W. H. 2003. Plant defense belowground and spatiotem- fields. Restoration Ecology 10:607–616. poral processes in natural vegetation. Ecology 84:2269–2280. Romig, D. E., M. J. Garlynd, and R. F. Harris. 1996. Farmer-based assess- Verhoef, H. A., and L. Brussaard. 1990. Decomposition and nitrogen ment of soil quality: a soil health scorecard. Pages 39–60 in J. W. mineralization in natural and agroecosystems—the contribution of Doran and A. J. Jones, editors. Methods of assessing soil quality. soil animals. Biogeochemistry 11:175–211. SSSA Special Publication No. 49. Soil Science Society of America, Vinton, M. A., and E. M. Goergen. 2006. Plant-soil feedbacks contribute Inc., Madison, Wisconsin. to the persistence of Bromus inermis in tallgrass prairie. Ecosystems Saxon, E., B. Baker, W. Hargrove, F. Hoffman, and C. Zganjar. 2005. 9:967–976. Mapping environments at risk under different climate change sce- Vosa´tka, M., J. Rydlova´, and R. Malcova´. 1999. Microbial inoculations of narios. Ecology Letters 8:53–60. plants for revegetation of disturbed soils in degraded ecosystems. Schwartz, M. W., J. D. Hoeksema, C. A. Gehring, N. C. Johnson, J. N. Pages 303–317 in P. Kova´r, editor. Nature and culture in landscape Klironomos, L. K. Abbott, and A. Pringle. 2006. The promise and ecology. Carolinum Press, Prague, Czech Republic. the potential consequences of the global transport of mycorrhizal Walker, R. F., S. B. McLaughlin, and D. C. West. 2004. Establishment of fungal inoculum. Ecology Letters 9:501–515. sweet birch on surface mine spoil as influenced by mycorrhizal ino- Scullion, J., and A. R. A. Mohammed. 1991. Effects of subsoiling and asso- culation and fertility. Restoration Ecology 12:8–19. ciated incorporation of fertilizer on soil rehabilitation after opencast Wardle, D. A. 2002. Communities and ecosystems: linking the above- mining for coal. Journal of Agricultural Science 116:265–273. ground and belowground components, Princeton University Press, Setala, H. 2002. Sensitivity of ecosystem functioning to changes in trophic Princeton, New Jersey. structure, functional group composition and in Wardle, D. A., R. D. Bardgett, J. N. Klironomos, H. Setala, W. H. van belowground food webs. Ecological Research 17:207–215. der Putten, and D. H. Wall. 2004. Ecological linkages between Setala, H., J. Laakso, J. Mikola, and V. Huhta. 1998. Functional diversity aboveground and belowground biota. Science 304:1629–1633. of organisms in relation to . Applied Wardle, D. A., and D. A. Peltzer. 2007. Aboveground-belowground link- Soil Ecology 9:25–31. ages, ecosystem development and ecosystem restoration. Pages Shepherd, G. 2000. Visual soil assessment: Vol. 1: field guide: cropping 45–68 in L. Walker, J. Walker, and R. Hobbs, editors. Linking resto- and pastoral grazing on flat to rolling country. Report no. ration and in theory and practice. Springer, 20/EXT/425, horizons.mw & Landcare Research, New Zealand. Heidelberg, Germany. Shimp,J.F.,J.C.Tracy,L.C.Davis,E.Lee,W.Huang,L.E.Erickson, Wardle, D. A., G. W. Yeates, R. N. Watson, and K. S. Nicholson. 1995. and J. L. Schnoor. 1993. Beneficial-effects of plants in the remedia- The detritus food-web and the diversity of soil fauna as indicators of tion of soil and groundwater contaminated with organic materials. disturbance regimes in agroecosystems. Plant and Soil 170:35–43.

616 Restoration Ecology DECEMBER 2008 Integrating Soil Ecological Knowledge

Whisenant, S. 1999. Repairing damaged ecosystems. Cambridge Univer- Xia, H. P. 2004. Ecological rehabilitation and phytoremediation with four sity Press, New York. grasses in oil shale mined land. Chemosphere 54:345–353. Wilson, S. D., and A. K. Gerry. 1995. Strategies for mixed-grass prairie Zak, D. R., W. E. Holmes, D. C. White, A. D. Peacock, and D. Tilman. restoration: herbicide, tilling, and nitrogen manipulation. Restora- 2003. Plant diversity, soil microbial communities, and ecosystem tion Ecology 3:290–298. function: are there any links? Ecology 84:2042–2050.

DECEMBER 2008 Restoration Ecology 617